Flora 238 (2018) 110–118 Contents lists available at ScienceDirect Flora j ournal homepage: www.elsevier.com/locate/flora How are endemic and widely distributed bromeliads responding to ଝ warming temperatures? A case study in a Brazilian hotspot ∗,1 1 ∗ Cleber Juliano Neves Chaves , Bárbara Simões Santos Leal , José Pires de Lemos-Filho Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil a r t i c l e i n f o a b s t r a c t Article history: The increase in mean global temperature is causing extensive changes in ecosystems. However, little Received 26 December 2016 is yet known about the heat tolerance of neotropical plant species. Here, we investigate heat tolerance Received in revised form 10 May 2017 variation in both restricted and widely distributed bromeliad species co-occurring in campo rupestre, a Accepted 13 May 2017 megadiverse ecosystem in central and eastern Brazil. We determined the heat tolerance of the photo- Edited by P. Morellato synthetic apparatus using chlorophyll fluorescence measurements to test if the endemic species Vriesea Available online 25 May 2017 minarum is more heat sensitive than two widely distributed species, Vriesea bituminosa and Aechmea nudicaulis. Furthermore, we tested if the distinct photosynthetic metabolisms of the species, sun expo- Keywords: sure, and rainfall seasonality of campo rupestre influence this outcome. Our results show that, contrary Thermal tolerance to our expectations, the endemic campo rupestre species did not show the greatest heat sensitivity, but Climate change Bromeliaceae did have one of the lowest heat tolerance plasticities. The CAM bromeliad A. nudicaulis was more heat Species range tolerant than the other bromeliad species, but both heat tolerance and its plasticity are highly affected by CAM sun exposure and the rainfall seasonality of campo rupestre. The low values and plasticity of V. minarum C 3 thermal tolerance could indicate that the threat of global warming could be greater for this campo rupestre endemic species. Our results also indicate that heat tolerance, especially the ability to withstand stressful temperatures for a long time, is an important parameter that differentiates the ecological strategies of these bromeliads species. © 2017 Elsevier GmbH. All rights reserved. 1. Introduction plasticity); developing new evolutionary strategies; changing their abundance and inter-specific interactions; and shifting their distri- ◦ ◦ Temperatures below 10 C and above 35 C can cause perma- bution (Holt, 1990; Parmesan, 2006; Blois et al., 2013; IPCC, 2014; nent damages to most plants (Went, 1953; Berry and Bjorkman, Parmesan and Hanley, 2015). Studies have suggested, for instance, 1980). The rise in the mean global temperature observed over the that some species have become restricted to refuges (see Rull, 2009; ◦ last century (IPCC, 2007) and an increase of ca. 2 C in the maxi- Stewart et al., 2010), shifting their ranges poleward and toward mum global temperature during the first half of the 21 st century higher elevations due to the warming temperatures since the last (IPCC, 2012) are causing deep alterations to ecosystems, from dam- glacial maximum (LGM; e.g., Parmesan and Yohe, 2003; Root et al., ages to the chloroplast integrity of plants (Berry and Bjorkman, 2003; Parmesan, 2006; Colwell et al., 2008; Rosenzweig et al., 2008; 1980; Yamane et al., 2000; Hüve et al., 2011; Zhang et al., 2012) Chen et al., 2011; Bässler et al., 2013; Pecl et al., 2017). Thus, species to mass extinctions (e.g. Crowley and North, 1987; Malcolm et al., currently restricted to interglacial refuges may be more sensitive 2006; Carpenter et al., 2008; Weigelt et al., 2016). But prior to to warming temperatures than widely distributed species. going extinct, species may respond to climate change by altering Due to its past climatic stability, the campo rupestre ecosystem their phenology and other physiological responses (i.e. phenotypic represents an example of interglacial refuge in the Neotropics (Bon- atelli et al., 2014; Barbosa et al., 2015). This vegetation complex is endemic to Brazil, and it is usually restricted to altitudes from 900 to over 2,000 ma.s.l., forming a mosaic archipelago-like system ଝ on low water-holding rocks of mountaintops surrounded by low- This article is part of a special issue entitled Plant life in campo rupestre: new lessons from an ancient biodiversity hotspot published at the journal FLORA 238C. lands (Alves et al., 2014; Silveira et al., 2016). Studies have shown ∗ Corresponding authors. that campo rupestre is probably the most ancient open vegetation E-mail addresses: [email protected] (C.J.N. Chaves), in eastern South America, comprising a great diversity and rate of [email protected] (B.S.S. Leal), [email protected] (J.P.d. Lemos-Filho). 1 endemism (Alves et al., 2014; Silveira et al., 2016). Nevertheless, Departamento de Ecologia, Instituto de Biociências, Universidade Estadual Paulista, São Paulo, Rio Claro, Brazil. recent studies indicate that campo rupestre vegetation could lose https://doi.org/10.1016/j.flora.2017.05.003 0367-2530/© 2017 Elsevier GmbH. All rights reserved. C.J.N. Chaves et al. / Flora 238 (2018) 110–118 111 from 44% (Bitencourt et al., 2016) to 95% (Fernandes et al., 2012) 2014a, 2014b). Therefore, it remains unclear how these plants will of its current area and about 25% of its angiosperm species due respond to ongoing climate change. to climate change (Bitencourt et al., 2016). Such reduction repre- Inferences about potential responses of species to climate sents the extinction of more than 400 microendemic plant species change from their current distribution can be a good strategy, since which are currently restricted to future unsuitable areas (Biten- some works report a strong relationship between ecological char- court et al., 2016). Such potential scenario is a consequence of the acteristics and niche projections (e.g. Thuiller et al., 2005; Garcia ◦ habitat reduction caused by a warming up to 5 C in temperature et al., 2014). Here, we aim to test whether an endemic bromeliad and an increase in frequency of extremely dry seasons. The low dis- species of campo rupestre is more sensitive to warming tempera- persal ability of most endemic species makes them unable to reach tures than species with wider distributions. For such, we measured other suitable mountains; and their high specialization level make the fluorescence of photosystem II through two methods: ramping them more sensitive to climate changes (Christensen et al., 2007; and static temperature assays. We also examine whether morpho- Dawson et al., 2011; Bittencourt et al., 2016). Despite these wor- physiological traits, such as photosynthetic pathways (i.e., CAM and rying forecasts, little is known about how these endemic species C3 photosynthesis), sun exposure, and the marked rainfall season- would respond to overcome the warming temperatures. ality of the campo rupestre, can bias the outcome. Finally, we test Bromeliaceae is one of the most representative plant families in whether heat tolerance and its plasticity can distinguish the eco- campo rupestre and nearly half of the bromeliad species occurring logical strategies of these bromeliads. in such environment are endemic (Versieux et al., 2008; Silveira et al., 2016). This family is also one of the best examples of adap- tive radiation in the Neotropics (Benzing, 2000; Givnish et al., 2. Material and methods 2014; Givnish, 2015; Palma-Silva et al., 2016). Crassulacean acid metabolism (CAM), for example, is often noted as a key innovation 2.1. Study site and plant species in the family that allowed the exploitation of arid environments, due to its mechanism that closes the stomata during the daytime This study was carried out in the Piedade Mountains (Serra da and avoids excessive water loss during dry periods (Givnish et al., Piedade), situated within the over-exploited Iron Quadrangle, in 2014; Silvestro et al., 2014; Palma-Silva et al., 2016). Global cli- the southern-most section of the core area of the campo rupestre matic changes may favor species with CAM metabolism, due to in the Espinhac¸ o Range, Eastern Brazil (Alves et al., 2014; Silveira their supposed higher thermal tolerance (e.g., Yamada et al., 1996; et al., 2016). The Piedade Mountains have a maximum altitude of Weng and Lai, 2005) and the anthropogenic increase of arid areas 1,746 ma.s.l., and the highest section presents a typical subtropi- (Nobel, 1988; Cushman and Borland, 2002; Mercier and Freschi, cal high-altitude climate, with a well-defined dry season between 2008; Osmond et al., 2008). However, Chaves et al. (2015) showed April and September, and the frequent occurrence of fog (Brandão that the daily organic acid accumulation of CAM plants has a strong and Gavilanes, 1990; Marques and Lemos-Filho, 2008). The sur- negative impact on their thermal tolerance (see also Yamori et al., roundings (Belo Horizonte city, 40 km from Serra da Piedade) show ◦ a well-defined dry season with an average temperature of 19 C and 6 mm of precipitation in the driest month, and a well-defined Fig. 1. Schematic representation of the distribution of Aechema nudicaulis, Vriesea bituminosa, and Vriesea minarum according the online database of the Global Biodiversity Information Facility (GBIF; via www.gbif.org). 112 C.J.N. Chaves et al. / Flora 238 (2018) 110–118 ◦ wet season, with an average temperature of 23 C and 322 mm of total precipitation in average on the wettest month (histori- cal data from January 1990 to December 2016 achieved in the ◦ website www.inmet.gov.br). Frosts and temperatures close to 0 C are common at the highest altitudes (Brandão and Gavilanes, 1990). Our study area is above 1,400 ma.s.l. and comprises two microenvironments: a xeric zone, highly exposed to sun and winds, characterized by the occurrence of iron-quartzite rock outcrops and herbaceous-shrubby vegetation (hereafter referred to as sun- exposed environment); and a shaded zone within an altitudinal cloud forest, characterized by the presence of shrubby and arboreal vegetation and high moisture (hereafter, shaded environment).